The physiology of a coelenterate neuromuscular synapse

Summary

• 1. Postsynaptic potentials can be recorded intracellularly from epitheliomuscular cells overlying the inner nerve-ring in the medusaPolyorchis penicillatus (Cnidaria, Hydrozoa) (Fig. 1). These postsynaptic potentials lead to the generation of muscle action potentials which propagate through the swimming-muscle sheets. It is the swimming motor neuron network that innervates this epithelium. An alternative motor pathway is present that involves a network of small, multipolar neurons that is interpolated between swimming motor neurons and overlying epithelial cells (Fig. 2).

• 2. That the postsynaptic potentials recorded are due to release of a chemical transmitter is supported by the following evidence: (a) PSPs have a constant delay$(\bar x = 3.2{\text{ms)}}$ following the presynaptic spike (Figs. 3, 4); (b) high Mg⁺⁺ concentrations reduce the amplitude of PSPs and eventually block transmission (Fig. 10); (c) there is no electrical coupling between presynaptic neurons and postsynaptic epithelial cells.

• 3. There is an inverse relationship between the duration of presynaptic action potentials and the amplitude of PSPs (Figs. 5, 6). The duration of presynaptic action potentials is a reflection of the degree of synchrony of spiking in the motor network so that short duration motor spikes are associated with synchronous firing. In such cases, the simultaneous release of transmitter substance at a number of neighbouring synapses will cause rapid temporal summation of PSPs in postsynaptic cells. Similarly, long duration presynaptic spikes are associated with asynchronous transmitter release and consequently with small PSPs (Figs. 8, 9).

• 4. Changes in PSP amplitude are seen in all postsynaptic cells of a localised region (Fig. 7).

• 5. The muscle action potential can be separated into two components, the velar and subumbrellar action potentials (Fig. 11). This biphasic nature of muscle action potentials recorded in the synaptic region results from all-or-none action potentials that are generated at the velar and subumbrellar borders of this region conducting back electrotonically. These action potentials made to conduct antidromically towards the synapses by electrical stimulation of the muscle sheets decrement as they travel through the synaptic region (Fig. 12). The nature of electrical coupling between epithelial cells in the synaptic non-muscular region and the muscle sheets proper must be different.

• 6. Larger amplitude PSPs are associated with muscle action potentials that follow with a shorter latency, and that have the two components (velar and subumbrellar) following each other more rapidly (Figs. 5, 9).

• 7. Action potentials in the motor network are brought into phase as they conduct around the margin. This leads to more synchronous activation of synapses and hence larger PSPs at regions distant from the initiation site of the motor spike. The resulting decrease in the latency of muscle APs at these distant sites will automatically compensate for the conduction delay of motor spikes.